Participatory innovation for human papillomavirus screening to accelerate the elimination of cervical cancer
Natalia M. Rodriguez
Abstract
On Nov 17, 2020, WHO launched a global strategy to accelerate the elimination of cervical cancer.1WHOGlobal strategy to accelerate the elimination of cervical cancer as a public health problem. World Health Organization, Geneva2020Google Scholar The strategy aims for all countries to achieve 90% human papillomavirus (HPV) vaccination coverage, 70% HPV screening coverage with a high-performance test, and 90% access to treatment for cervical pre-cancer and cancer by 2030. Despite being a preventable and treatable disease, cervical cancer remains one of the most serious threats to women's lives globally, and is a marker of health disparity and limited health-care access.2Knaul FM Rodriguez NM Arreola-Ornelas H Olson JR Cervical cancer: lessons learned from neglected tropical diseases.Lancet Glob Health. 2019; 7: e299-e300Summary Full Text Full Text PDF PubMed Scopus (6) Google Scholar Screening is crucial to successful cervical cancer management because HPV infection is asymptomatic, progression of precancerous lesions is slow, and treatment of advanced disease can be challenging and costly. However, screening rates remain low in areas of poverty and marginalisation, even in high-income countries.3Gakidou E Nordhagen S Obermeyer Z Coverage of cervical cancer screening in 57 countries: low average levels and large inequalities.PLoS Med. 2008; 5: e132Crossref PubMed Scopus (328) Google Scholar In the USA, for example, the Healthy People 20204Centers for Disease Control and PreventionNational Center for Health StatisticsNational Health Interview Survey.https://www.healthypeople.gov/2020/data-search/Search-the-Data#topic-area=3513Date: 2008–2018Date accessed: November 23, 2020Google Scholar target of 93% cervical cancer screening coverage was not met, reaching only 80·5% in 2018. Screening rates decreased by 4% between 2008 and 2018, and screening coverage disparities persisted, including among uninsured people (61% screened), foreign-born immigrants (75% screened), people who completed less than high school education (71% screened), and people living in poverty (70% screened).4Centers for Disease Control and PreventionNational Center for Health StatisticsNational Health Interview Survey.https://www.healthypeople.gov/2020/data-search/Search-the-Data#topic-area=3513Date: 2008–2018Date accessed: November 23, 2020Google Scholar The full impact of the COVID-19 pandemic on cancer screening is not yet known, but substantial drops in screening rates continue, with disproportionate effects on disadvantaged groups.5Sharpless NE COVID-19 and cancer.Science. 2020; 3681290Crossref PubMed Scopus (95) Google Scholar Accompanying the global strategy, newly released WHO guidance6WHOIntroducing and scaling up testing for human papillomavirus as part of a comprehensive programme for prevention and control of cervical cancer: a step-by-step guide. World Health Organization, Geneva2020Google Scholar on introducing and scaling up HPV testing for prevention and control of cervical cancer includes important considerations around building the right delivery model by "selecting testing strategies that will reach the target population" and "strongly considering community health care supported models using self-sampling".6WHOIntroducing and scaling up testing for human papillomavirus as part of a comprehensive programme for prevention and control of cervical cancer: a step-by-step guide. World Health Organization, Geneva2020Google Scholar To achieve cervical cancer screening coverage targets, simultaneous and strategic innovation is needed both technologically (new and better tools) and at delivery (better ways of implementing these tools). WHO currently recommends HPV testing as a primary cervical cancer screening tool for women older than 30 years, where resources permit, and 2020 American Cancer Society guidelines6WHOIntroducing and scaling up testing for human papillomavirus as part of a comprehensive programme for prevention and control of cervical cancer: a step-by-step guide. World Health Organization, Geneva2020Google Scholar, 7Fontham ET Wolf AM Church TR et al.Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society.CA Cancer J Clin. 2020; 70: 321-346Crossref PubMed Scopus (76) Google Scholar included a shift to primary HPV testing, without cytology, as the preferred screening method. Only two devices for primary HPV screening are approved by the US Food and Drug Administration (FDA; cobas HPV [Roche Molecular Diagnostics, Pleasanton CA] and Onclarity HPV [BD Diagnostics, Sparks MD]), both of which require laboratory infrastructure and batch testing that can take hours. Rapid, single-use, molecular HPV tests could enable community-based testing with self-collected samples, circumventing many of the barriers to existing tests. Non-batch point-of-care tests, such as Xpert HPV (Cepheid, Sunnyvale CA), bring us a step closer to community-based testing. However, these tests still rely on laboratory and electricity-dependent platforms, and are not yet approved by the FDA.8Sayed S Chung M Temmermans M Point-of-care HPV molecular diagnostics for a test-and-treat model in high-risk HIV populations.Lancet Glob Health. 2020; 8: e171-e172Summary Full Text Full Text PDF PubMed Scopus (6) Google Scholar Machine-learning-based approaches and digital cytology, especially in the age of telehealth, also show promising preliminary results and should undergo urgent validation.9Hu L Bell D Antani S et al.An observational study of deep learning and automated evaluation of cervical images for cancer screening.J Natl Cancer Inst. 2019; 111: 923-932Crossref PubMed Scopus (102) Google Scholar However, technological innovation alone is rarely the answer. The process of successful uptake, adoption, and diffusion of new technologies into health systems, especially in low-resource settings, is poorly understood and often excludes the perspective of the end user or meaningful consideration of community, social structure, and cultural context. Human-centred design approaches to identify critical context-specific functional, systemic, and user requirements are essential. Furthermore, delivery strategies must consider the persistent sociocultural access barriers that exacerbate health disparities among low-income, uninsured, immigrant, and racial minority groups that are often marginalised and medically underserved. These include barriers related to the social determinants of health, low health literacy, reluctance to have a pelvic evaluation, stigma associated with sexually transmitted diseases like HPV, and cultural family dynamics potentiating risk of gender-based violence or abandonment after diagnosis. Community-engaged approaches are needed to better understand and address these barriers. Community-based participatory research, for example, invites community stakeholder participation throughout the research process and has led to innovative delivery interventions that increased cervical cancer screening among high-risk populations, such as HPV self-sampling delivered by community health workers.10Barbee L Kobetz E Menard J et al.Assessing the acceptability of self-sampling for HPV among Haitian immigrant women: CBPR in action.Cancer Causes Control. 2010; 21: 421-431Crossref PubMed Scopus (68) Google Scholar As shown by decades of HIV and malaria testing in sub-Saharan Africa,11Counihan H Harvey SA Sekeseke-Chinyama M et al.Community health workers use malaria rapid diagnostic tests (RDTs) safely and accurately: results of a longitudinal study in Zambia.Am J Trop Med Hyg. 2012; 87: 57-63Crossref PubMed Scopus (82) Google Scholar, 12Mwai GW Mburu G Torpey K Frost P Ford N Seeley J Role and outcomes of community health workers in HIV care in sub-Saharan Africa: a systematic review.J Int AIDS Soc. 2013; 1618586Crossref PubMed Scopus (181) Google Scholar community health workers can be instrumental to the acceptance and adoption of a screening test, but they must be appropriately trained and included, along with the target community, in the actual design of the technology. Moreover, implementation of an HPV test is more complex than are those for HIV or malaria, because a positive result does not necessarily indicate cervical cancer, but rather a higher risk that requires further testing. Successful adoption of a screening technology thus requires engagement of diverse stakeholders, including health-care providers, in both the design and implementation processes, to ensure follow-up testing and linkage to care. Participatory approaches such as community-based participatory research and human-centred design are powerful tools that enable the technological and delivery innovations needed to implement the WHO global strategy, reach the most vulnerable worldwide, and eliminate cervical cancer in every context once and for all. I have a patent pending (application no. 16/061,129) for a platform device that combines nucleic acid extraction, amplification, and detection to enable rapid testing with visual readout. I thank Erin Kobetz and Jose Jeronimo for fruitful conversations and insights on this topic and funding through the National Cancer Institute of the National Institutes of Health under Award Number K01CA241073. The content is solely the responsibility of the author and does not necessarily represent the official views of the National Institutes of Health.